The pattern of apolipoprotein A-I lysine carbamylation reflects its lipidation state and the chemical environment within human atherosclerotic aorta

J Biol Chem. 2022 Apr;298(4):101832. doi: 10.1016/j.jbc.2022.101832. Epub 2022 Mar 15.

Abstract

Protein lysine carbamylation is an irreversible post-translational modification resulting in generation of homocitrulline (N-ε-carbamyllysine), which no longer possesses a charged ε-amino moiety. Two distinct pathways can promote protein carbamylation. One results from urea decomposition, forming an equilibrium mixture of cyanate (CNO-) and the reactive electrophile isocyanate. The second pathway involves myeloperoxidase (MPO)-catalyzed oxidation of thiocyanate (SCN-), yielding CNO- and isocyanate. Apolipoprotein A-I (apoA-I), the major protein constituent of high-density lipoprotein (HDL), is a known target for MPO-catalyzed modification in vivo, converting the cardioprotective lipoprotein into a proatherogenic and proapoptotic one. We hypothesized that monitoring site-specific carbamylation patterns of apoA-I recovered from human atherosclerotic aorta could provide insights into the chemical environment within the artery wall. To test this, we first mapped carbamyllysine obtained from in vitro carbamylation of apoA-I by both the urea-driven (nonenzymatic) and inflammatory-driven (enzymatic) pathways in lipid-poor and lipidated apoA-I (reconstituted HDL). Our results suggest that lysine residues within proximity of the known MPO-binding sites on HDL are preferentially targeted by the enzymatic (MPO) carbamylation pathway, whereas the nonenzymatic pathway leads to nearly uniform distribution of carbamylated lysine residues along the apoA-I polypeptide chain. Quantitative proteomic analyses of apoA-I from human aortic atheroma identified 16 of the 21 lysine residues as carbamylated and suggested that the majority of apoA-I carbamylation in vivo occurs on "lipid-poor" apoA-I forms via the nonenzymatic CNO- pathway. Monitoring patterns of apoA-I carbamylation recovered from arterial tissues can provide insights into both apoA-I structure and the chemical environment within human atheroma.

Keywords: apolipoprotein A-I; carbamylation; cardiovascular disease; cyanate; high-density lipoprotein; homocitrulline; myeloperoxidase; oxidation; urea.

MeSH terms

  • Aorta* / metabolism
  • Aorta* / pathology
  • Apolipoprotein A-I* / metabolism
  • Atherosclerosis* / metabolism
  • Atherosclerosis* / pathology
  • Humans
  • Isocyanates
  • Lipoproteins, HDL / metabolism
  • Lysine* / metabolism
  • Plaque, Atherosclerotic / pathology
  • Protein Carbamylation*
  • Proteomics
  • Urea

Substances

  • Apolipoprotein A-I
  • Isocyanates
  • Lipoproteins, HDL
  • Urea
  • Lysine